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Flowers of Araliaceae: Structural diversity, developmental and evolutionary

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E Plant Div. Evol. Vol. 128/1–2, 247–268
Stuttgart, August 20, 2010

Flowers of Araliaceae: structural diversity,

developmental and evolutionary aspects
By Maxim S. Nuraliev, Alexei A. Oskolski, Dmitry D. Sokoloff and
Margarita V. Remizowa

With 37 figures

Abstract

Nuraliev, M.S., Oskolski, A.A., Sokoloff, D.D. & Remizowa, M.V.: Flowers of Araliaceae: structural
diversity, developmental and evolutionary aspects. — Plant Div. Evol. 128: 247–268. 2010. — ISSN
1869-6155.

Within Araliaceae, at least four groups are recognized to have significant deviations from the typical
euasterid flower groundplan: (1) Asian Schefflera clade (incl. Tupidanthus), (2) Plerandra group, (3)
Tetraplasandra and (4) Osmoxylon. The main trends of flower structure variation are: reduction of
calyx, increase in number of stamen whorls, increase of overall flower merism or only of stamen
number, increase or decrease of carpel number, congenital petal fusion with postgenital corolla clo-
sure into a massive calyptra, appearance of flower disymmetry or asymmetry during flower develop-
ment or even from its very beginning. Loss of polysymmetry is strongly correlated with increase of
organ number, at least in the androecium and in the gynoecium. Other trends show mosaic distribution
between taxa studied. Our data suggest primitiveness of pentamerous tetracyclic polysymmetric flow-
ers (possibly with dimerous gynoecium) in Araliaceae and multiple losses of this floral construction
in the evolution of the family. Multistaminate and multicarpellate flowers are clearly derived types in
Araliaceae.

Keywords: Apiales, Araliaceae, flower polymery, flower groundplan, evolution.

Introduction
Araliaceae is a family of euasterids II (APGII 2003) closely related to Umbelliferae.
This relationship was stated by many researchers on the basis of morphological data
(e.g., Bentham & Hooker 1863, Wettstein 1924, Hutchinson 1959, Melchior 1964,
Takhtajan 1966, 1987, Cronquist 1981, 1988) and supported by molecular phylogenet-
ics (e.g. Plunkett et al. 2004a). These two families represent the vast majority of spe-
cies in the order Apiales sensu APGII (2003) and Plunkett et al. (2004a). As well as for
many other eudicots, polysymmetric tetracyclic pentamerous (often except the gynoe-
cium) flowers are considered to be typical for Apiales. In contrast to many other as-
terids, presence of a corolla tube is rare in Apiales. Umbelliferae are generally charac-

Received January 13, 2009, in revised form April 20, 2009, accepted April 23, 2009

© 2010 E. SchweizerbartÕ sche Verlagsbuchhandlung, Stuttgart, Germany www.schweizerbart.de

DOI: 10.1127/1869-6155/2010/0128-0012 1869-6155/2010/0128-0012 $ 05.50

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248 M.S. Nuraliev et al., Flowers of Araliaceae

terized by low variation of mature flower structure (e.g., Drude 1898, Erbar & Leins
1997, Leins & Erbar 2004), that is why systematics of this group was mainly based on
fruit morphology and anatomy (e.g., Hoffmann 1814, Drude 1898). As pointed out by
Cronquist (1981), “all of the features that have been used to distinguish the Apiaceae
as a family can be found individually in Araliaceae”. This is evidence of their closest
relationships and the reason of difficulties with delimitation of these families (Bau-
mann 1946, Pervukhina 1953, Tikhomirov 1961, Plunkett et al. 2004a). In contrast to
Umbelliferae, flower morphology of Araliaceae is extremely diverse; moreover, many
species of this family possess flowers that are unusual for euasterids due to their re-
markable variation in merism and other crucial characters of the flower groundplan
(Harms 1898, Melchior 1964, Philipson 1970, Eyde & Tseng 1971). Floral morphol-
ogy of these species of Araliaceae caused a discussion on the ancestral flower structure
for the order Apiales (reviewed in Eyde & Tseng 1971).
Before the middle of the XXth century it was commonly accepted that the higher
the number of elements in the flower, the more primitive it is. Hence, most of the ara-
liaceous genera with polymerous flowers (Tetraplasandra, Plerandra and Tupidan-
thus) were grouped together and put at the base of the family Araliaceae and the order
Apiales (or Umbellales in Li 1942). Cronquist (1968, 1981) was the first to consider
polymerous araliaceous flowers as derived from pentamerous ones. Eyde and Tseng
(1971) suggested that the ancestral flower of Araliaceae was slightly polymerous and
most of Araliaceae were evaluated to have pentamerous flower, while several genera,
e.g. Plerandra, Tetraplasandra and Tupidanthus, underwent secondary polymeriza-
tion. Takhtajan (1997) fully agreed with Cronquist in the statement that polymerous
types probably underwent a secondary increase in the number of parts, but pointed out
that polymerization occurred basically in the archaic genera of the family, such as
Tupidanthus, Schefflera and Tetraplasandra.
Molecular phylogenetic data (Wen et al. 2001, Plunkett et al. 2004b) support the
idea of secondary origin of polymerous flowers within Araliaceae. Mapping of flower
merism on the molecular phylogenetic tree shows that species with polymerous flow-
ers are scattered among species with pentamerous flowers. This means that flower
polymery appeared independently several times within the family. However, the evo-
lutionary pathways that led to such an unusual phenomenon are still unclear.
The present study is focused on the structural diversity of polymerous flowers with-
in Araliaceae. We compare different evolutionary lineages within this family to under-
stand differences in patterns of variation of different features of flower architecture.
Furthermore, we are interested in elucidating possible correlations between variations
of different characters.
We have examined three groups of Araliaceae which are remarkable in their
polymerous flowers. The first group is the so-called Asian Schefflera clade (Plunkett et
al. 2005), a monophyletic group of Asian (and some Australian) species of a huge
polyphyletic genus Schefflera and some segregate genera, such as Tupidanthus. This
clade includes many species with ordinary pentamerous flowers as well as several taxa
with polymerous flowers (e.g., Tupidanthus). According to molecular phylogenetics,
Tupidanthus calyptratus is closely related to Schefflera subintegra (M.S. Nuraliev,
G.V. Degtjareva et al., unpubl. data). This species with polystemonous (16–27 sta-

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 M.S. Nuraliev et al., Flowers of Araliaceae 249

mens) flowers was formerly placed in a separate genus Scheffleropsis that is most
similar to Tupidanthus in its floral morphology (Grushvitsky & Skvortsova 1973).
Schefflera actinophylla, another close relative of Tupidanthus, belongs to the Brassaia
group of Schefflera, which is also characterized by polymerous flowers (their merism
varies from 10 to 30 — Frodin 1975).
The second group is the genus Tetraplasandra that is interesting for its polymerous
androecium and variable (inferior to superior) ovary position. According to the molecu-
lar data, Tetraplasandra is nested within the Polyscias s.l. clade (Plunkett et al. 2004b).
Tetraplasandra gymnocarpa is the only species of Araliaceae with a fully superior
ovary. Such an unusual ovary position for Apiales is derived from the (semi)inferior
condition (Eyde & Tseng 1969, Costello & Motley 2004). Costello and Motley (2004)
found that the ovary becomes superior only at the latest stages of flower development,
whereas earlier the ovary resembles that of Tetraplasandra species with (semi)inferior
ovary. Moreover, a polymerous androecium of two whorls has been reported (Lowry
1990) at least in two species of Tetraplasandra (T. waialealae and T. waimeae).
The third group examined here is the genus Plerandra which is remarkable by its
numerous stamen whorls. As recent molecular phylogenetic studies show, Plerandra
is placed in the Melanesian Schefflera clade (Plunkett et al. 2004b, Plunkett & Lowry
2008). Whereas most species of this clade belonging to the informal subgroups “Cana-
coschefflera”, “Gabriellae” and “Dizygotheca” share pentamerous flowers, the mem-
bers of Plerandra and the closely related subgroup “Dictyophlebes” show an increase
in number of the androecium whorls from one (Schefflera costata, Plerandra bakeri-
ana) to seven (P. pickeringii) together with increase of the stamen number in each
whorl. As a result, the flower of P. pickeringii contains up to 500 stamens (Smith &
Stone 1968); this is the most extremely polystemonous androecium within euasterids.

Material and methods

Gross morphology and development of flowers for the following species have been examined: Schef-
flera venulosa (Wight & Arnott) Harms (collected from cultivated plants in Tsitsin Main Botanical
Garden of the Russian Academy of Sciences, Moscow, in 2005, and in Komarov Botanical Institute,
St.-Petersburg, in 2007 and 2008); Schefflera octophylla (Loureiro) Harms (collected in Fairy Lake
Botanical Gardens, Shenzhen, China, in 2005); Schefflera actinophylla (Endl.) Harms (collected from
cultivated plants in Fairy Lake Botanical Gardens, Shenzhen, China, 2005, and in Johannesburg,
South Africa, 2007); Tupidanthus calyptratus J.D. Hooker & Thomson (collected by A.L. Takhtajan
and Le Kim Bien, no. 8423 on 19.01.1975 in the province Lai Chau, Vietnam, and from plants culti-
vated in San Diego, California); Tetraplasandra waialealae (collected by David H. Lorence no. 9542,
04.04.2007 in Kauai, Hawaii); Plerandra insolita A.C. Sm., Plerandra grandiflora A.C. Sm., and
Plerandra victoriae Gibbs (collected by Gregory M. Plunkett [his voucher’ numbers 1834, 1939,
1909 correspondingly] in 2005 in Fiji).
Flowers at various developmental stages were fixed in FAA or 70% ethanol and stored in 70%
ethanol. For scanning electron microscopy (SEM), parts of inflorescences and flowers were dehy-
drated in 100% ethanol and 100% acetone. Dehydrated material was critical-point dried and sputter-
coated with Pt/Pd. For light microscope observations, material was sectioned using standard methods
of paraffin embedding and serial sectioning at 15 μm thickness (Barykina et al. 2004). Sections were
stained in picroindigocarmine and carbolic fuchsine (Axenov 1967) and mounted in Canadian bal-
sam.

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250 M.S. Nuraliev et al., Flowers of Araliaceae

Results
Asian Schefflera clade. We distinguish four main types of flower groundplan within
this group:
1. Many Schefflera species from this group including S. venulosa (Fig. 1–6) possess
typical araliaceous flowers which are tetracyclic, pentamerous, with semi-inferior ova-
ry. Elements of the adjacent whorls alternate with each other (Fig. 1, 3). Flowers typi-
cally consist of five inconspicuous sepals fused congenitally at their bases, five free
petals with apices curved down toward the gynoecium, five stamens and five united
carpels that form an asterisk-shaped compitum (Fig. 19).
2. In Schefflera octophylla (Fig. 7–12), flowers differ from typical araliaceous flow-
ers in some crucial characters. In mature flowers, calyx is well-developed and forms a
massive tube with short free lobes (Fig. 9, 12). The gynoecium is polymerous and usu-
ally consists of 8 (6 to 9) carpels. The style is slightly elliptic rather than circular in
cross-section (Fig. 7–10). Although the merism of the gynoecium is increased, the ca-
lyx, the corolla, and the androecium form three regularly alternating pentamerous
whorls.
3. Schefflera actinophylla (Fig. 13–18) usually possesses 12-merous flowers. Mer-
ism of different whorls within a flower is not necessarily equal. The calyx is repre-
sented by a thin rim at the upper receptacle edge and clearly visible only in SEM im-
ages (Fig. 17, 18). In mature flowers, this rim is absolutely homogenous and bears no
traces of sepal apices. Unfortunately, we did not study calyx development because of
the absence of appropriate material. Another unusual feature of the S. actinophylla
flowers is a change of symmetry in the course of flower development. In the beginning
of flower development, the receptacle is clearly circular in outline (Fig. 13, 14). After
elongation of the symplicate zone, however, the carpels in some flowers do not appear
to be equally spaced from the flower centre. Rather, they are arranged in two rows
along a line, so that the top of the gynoecium is elliptic in cross-section in the mature
flowers (Fig. 16). This pattern of carpel arrangement results in a modified elongated
shape of pollen tube transmitting tissue in cross-section at the level of the compitum
(Fig. 20). The whole flower usually also becomes slightly elliptic in outline. Similar to
the carpels, the petals are arranged in two rows along a line in a flower bud viewed
from the top (Fig. 15). As a result, the mature flowers are weakly disymmetric. The
plane of the flower symmetry is randomly oriented in relation to flower position with
respect to its subtending bract and the main axis.
4. The flower structure of Tupidanthus calyptratus is described in detail in Sokoloff
et al. (2007). The flower is peculiar in its incredibly high merism of gynoecium and
androecium (up to 200 elements in each whorl; Grushvitsky 1981, Wen et al. 2001),
folded butterfly-like shape of receptacle, which is recognizable from the earliest stages
of floral development, and carpels arranged along a branched H-shaped or more com-
plex pattern (see Fig. 1–69 in Sokoloff et al. 2007). The calyx forms an inconspicuous
rim. The corolla forms a tube in which no evidence of petal boundaries can be traced.
It is initiated as a continuous rim and its vasculature does not allow determining petal
number (Nuraliev et al., 2009). Hence, there is no method available to distinguish pet-
als from each other and to establish corolla merism of Tupidanthus. The orifice of the

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 M.S. Nuraliev et al., Flowers of Araliaceae 251

Fig. 1–6. Schefflera venulosa. This species typically possesses pentamerous flowers. As in some other
species of Schefflera, flowers of S. venulosa are either hermaphroditic or functionally female (Nuraliev
et al. 2009). — 1, Young flower with young sepals and petals, a rare case of a tetramerous flower. —
2, Almost mature hermaphroditic flower, corolla removed. — 3, Mature functionally female pentam-
erous flower. — 4, A rare case of hexamerous gynoecium in a functionally female flower. — 5, Lon-
gitudinal section of mature functionally female flower with visible calyx (arrows). — 6, Transversal
section of a six-loculed ovary. — pet = petal, sep = sepal, st = stamen, stig = stigma.

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252 M.S. Nuraliev et al., Flowers of Araliaceae

Fig. 7–12. Schefflera octophylla. This species is characterized by pentamerous perianth and androe-
cium and polymerous gynoecium. — 7, Young gynoecium of 7 carpels. — 8, Young gynoecium of 6
carpels. 9, — Mature flower, corolla and one of the stamens removed; note the well-developed calyx
tube (arrow). — 10, Mature stigmas. 11, Mature corolla, top view. — 12, A longitudinal section of
mature flower; note the calyx tube (arrows). — pet = petal, sep = sepal, st = stamen, stig = stigma.

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 M.S. Nuraliev et al., Flowers of Araliaceae 253

Fig. 13–18. Schefflera actinophylla: polymerous (hemi)isomerous flowers. — 13, Young flower at the
beginning of gynoecium development, corolla partially removed; note the receptacle is circular in
outline. — 14, Flower at slightly later stage; note numerous free petals. — 15, Almost mature corolla
in top view; petals tend to meet each other along a line. — 16, Mature gynoecium; carpels meet each
other along a line. — 17, Mature calyx (arrow), a petal and a stamen are removed. — 18, A longitudi-
nal section of mature flower; note the inconspicuous calyx (arrow) at the base of the corolla. — pet =
petal, st = stamen, stig = stigma.

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254 M.S. Nuraliev et al., Flowers of Araliaceae

Fig. 19–20. Cross sections of mature Scheffflera spp. flowers at compitum level (asterisks). —
19, Schefflera venulosa, compitum is star-shaped. — 20, Schefflera actinophylla, compitum is oval.
— pet = petal, st = stamen.

congenitally developed corolla tube postgenitally closes, and the corolla forms a thick
calyptra.
It is important to note that in the Asian Schefflera species the flower merism is often
variable at infraspecific level. For example, in S. venulosa we observed several tetram-
erous and hexamerous flowers. The merism of S. actinophylla flowers varies from 11
to 14. Highly polymerous flowers of T. calyptratus can bear 50 to 130 (200) stamens
and carpels.
Flowers of Tetraplasandra waialealae (Fig. 21–30) possess a polymerous andr-
oecium combined with oligomerous corolla and gynoecium. Our material does not
allow examining the sequence of organ initiation, but contains some relatively early
stages with very young carpels and stamens. The calyx of T. waialealae forms a rela-
tively massive but shallow cup with almost entire margin (Fig. 21, 28). Precise count-
ing of sepals is problematic. Petal number varies in our material between six and seven
(Fig. 21, 26, 28–30). In some flowers, a petal is much narrower than the other petals.
Petal aestivation is valvate. The petals are initiated as separated primordia, which fuse
postgenitally by their margins in the course of floral development. The petals of young
flowers are massive, with tips curved inwards (Fig. 30). Petal tips are in close contact
with the young gynoecium in flower buds, and the space allowed for packing young
stamens is clearly visible as an undulating furrow in the inner side of a removed co-
rolla. In anthetic flowers the petals are expanded separately forming no calyptra.
At least 28–46 stamens are arranged in a single whorl. The one-whorled condition
is especially clear in the youngest flowers (Fig. 21, 22, 24, 25, 27, 28). Stamens in-
serted on the radii where adjacent petals join each other (alternipetalous stamens) are
just slightly more distant from the floral centre than the antepetalous stamens and the
shape of stamen whorl appears to be wavy (Fig. 21, 26). Probably, such arrangement
of stamens is caused by the shape of the petal bases, which are thicker in their middle
parts than near their margins. The number of the antepetalous stamens located in front

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 M.S. Nuraliev et al., Flowers of Araliaceae 255

Fig. 21–26. Tetraplasandra waialealae: flowers with polymerous androecium. — 21, Developing
flower with corolla removed. — 22, Developing androecium and gynoecium; note carpels alternating
with petals. — 23, Developing flower with corolla removed, the androecium whorl is folded. — 24.
Developing flower with one distinct stamen whorl, note two of six alternipetalous stamens are very
large. — 25, Developing gynoecium and part of androecium; note the upper carpel clearly alternates
with petals. — 26, Developing flower with corolla removed, the androecium whorl is folded.

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256 M.S. Nuraliev et al., Flowers of Araliaceae

Fig. 27–30. Tetraplasandra waialealae. — 27, Developing flower with corolla removed and pentam-
erous gynoecium. — 28, Developing flower with corolla removed; carpels neither alternate with pet-
als nor are strictly opposite the petals. — 29, Almost mature corolla in top view. — 30, Almost mature
corolla in inside view, note the involute petal apices. — pet = petal, stig = stigma.

of a petal is not stable and can vary within a flower (minimum number is two). At
early stages before thecal differentiation, the alternipetalous stamens are often larger
than the antepetalous ones (Fig. 24). It is tempting to explain this by the fact that the
alternipetalous stamens are first to initiate during the androecium development. In
some young flowers, however, only few alternipetalous stamens are large, whereas
others are of the same size as the antepetalous ones. Occasionally, some of alternipeta-
lous stamens are extremely large (up to six times larger than other stamens); these
cases are probably abnormalities in stamen development.
At later developmental stages, the androecium whorl becomes considerably crowd-
ed in a waveline (Fig. 23, 26). The number of outer and inner bends is equal to petal

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 M.S. Nuraliev et al., Flowers of Araliaceae 257

number, with alternipetalous stamens occurring on the tip of the waveline. Apart from
folding of the entire whorl, the anthers of the adjacent stamens overlap each other be-
cause the anthers are wider than the space allowed for a stamen. This gives the false
impression of more than one androecium whorl.
Carpel number varied in our material between five and seven (Fig. 21–28). When
carpel number was the same as the petal number (which was not always the case), the
carpels occured either in the same radii as the petals, or in the radii alternating with
those of the petals.
A remarkable feature of Plerandra (Fig. 31–36) is a concave, cup-like receptacle
(Fig. 31, 32). In contrast to the presence of polymerous whorls (i.e., with more than five
elements) in androecium and gynoecium, the perianth of Plerandra is oligomerous, at
least in the examined species. The calyx is typically pentamerous, with sepal bases
united in a more or less pronounced tube. Five valvate petals are massive and coherent
in young flowers; they expand separately in anthetic flowers, forming no calyptra.
In P. insoluta and P. victoriae, the flowers bear three whorls of stamens with about
30 stamens in each whorl and one whorl of ten carpels (Fig. 33, 36). Flowers of P. gran-
diflora bear two whorls of stamens with 20–25 stamens in a whorl and a gynoecium
with eight or nine carpels (Fig. 34, 35). The outline of each stamen whorl sometimes
can be slightly wavy (Fig. 33). Adjacent stamen whorls can slightly differ in the num-
ber of stamens in Plerandra. Initiation of the stamen whorls proceeds on the concave
receptacle in basipetal (i.e., morphologically centripetal) sequence. Alternating stamen
position in adjacent whorls was not always obvious. At least in some cases, adjacent
stamens of different whorls where clearly on the same radius.

Discussion

Trends in the variation of flowers of Araliaceae

Looking over the variability of araliaceous flowers described above, the following
trends in variation in the flower groundplan can be recognized:
1. Variation in whorl number.
(A) Reduction of the calyx up to its complete loss. A well-developed calyx (such as
in Schefflera octophylla and in species of Plerandra) is not common within Araliaceae.
Usually, the calyx is much smaller than the corolla; it can form a short tube with free
sepal apices (most of Schefflera species). In most polymerous flowers, (e.g., in Os-
moxylon (Philipson 1979), S. actinophylla and T. calyptratus) the calyx is represented
by an inconspicuous rim with no traces of sepal apices. Thus, there is an apparent cor-
relation between flower polymery and calyx reduction. However, the calyx is absent
(from the earliest developmental stages) in pentamerous flowers of Hydrocotyle (Erbar
& Leins 1985). Furthermore, this feature can be found among Umbelliferae and even
among its subfamily Apioideae with remarkably stable flower structure, for instance,
in the genus Chaerophyllum (Erbar & Leins 1997, Leins & Erbar 2004, Sokoloff et al.
2008).
(B) Increase in number of stamen whorls constantly occurs in different species of

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258 M.S. Nuraliev et al., Flowers of Araliaceae

Fig. 31–36. Plerandra spp., a rare case of polycyclic androecium among Apiales. — 31, P. victoriae,
the very beginning of androecium development; note the concave floral apex. — 32, P. victoriae, sta-
men initiation. — 33, P. victoriae, young flower, corolla removed. — 34, P. grandiflora, androecium
and gynoecium development. — 35, P. grandiflora, young flower, corolla removed. — 36, P. insoluta,
young androecium and gynoecium.

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 M.S. Nuraliev et al., Flowers of Araliaceae 259

Plerandra. This is the only clearly documented case of a polycyclic androecium among
Araliaceae. Lowry (1990) reported two whorls of stamens in Tetraplasandra waialea-
lae and T. waimeae, but his data are not confirmed by our results at least for the former
species. Lowry did not examine, however, the early developmental stages, in which the
one-whorled condition was especially clear in our material. More data are needed (es-
pecially for T. waimeae) to clarify the occurrence of a two-whorled androecium in
Tetraplasandra.
As outlined above, a regular alternation of the members of adjacent stamen whorls
is not always obvious in Plerandra. Therefore, one might speculate that stamen ar-
rangement is chaotic rather than whorled in Pleranrda. Though only limited material
of Plerandra was available for our study, we believe that the stamens generally follow
arrangement in several tiers and the arrangement can be called whorled. The irregu-
larities in alternation of the adjacent whorl members may be due to increased merism,
which often leads to partial isomery (see below). An important observation made in
our study is the absence of any traces of the common stamen primordia or a ring pri-
mordium in Plerandra. Floral vascular anatomy (Philipson 1970) shows absence of
stamen trunk bundles in Plerandra.
The presence of more than one stamen whorl is an extremely rare condition for
euasterids. Apart from Plerandra, it is reported from Dialypetalanthus (Piesschaert et
al. 1997), which is now placed in Rubiaceae (Piesschaert et al. 1997, Fay et al. 2000,
APG II 2003). However, stamen initiation was not documented so far in Dialypetalan-
thus, and the conclusion on presence of two whorls is inferred from observations of
mature flowers only. Another possible euasterid member with several whorls of sta-
mens is Hoplestigma. This genus was unplaced because of lack of the robust molecular
phylogenetic data (see APG II 2003), but its position in or near Boraginaceae is most
likely (e.g., Takhtajan 1997), and new molecular data support this conclusion (Stevens
2009; M.W. Chase, pers. comm.). Although the multistaminate androecium of Hoples-
tigma is described as polycyclic (e.g., Goldberg 1986), this state is not clear enough
from the published illustrations, and developmental data are apparently absent.
Though a polycyclic androecium is very rare among euasterids, it occurs in some
members of the two basal asterid orders, viz. Ericales and Cornales. Polycyclic polys-
temony is documented in Hydrangeaceae and Loasaceae (Cornales) and in 10 of 23
families of Ericales (e.g. Hufford 1998, Endress 2002, Schönenberger & Grenhagen
2005).
Another feature of Plerandra that is unusual for euasterids is stamen formation on
a markedly concave receptacle. This condition, however, could be correlated with
polycycly of the androecium, because invagination of the receptacle provides the space
necessary to arrange multiple stamen whorls. Multiple stamen whorls initiating on the
concave receptacle in the basipetal (i.e., morphologically centripetal) sequence is
known in many groups of rosids (e.g., Leins 1964, Ronse De Craene & Smets 1991,
Ronse De Craene 1992). The same pattern of polyandry is also found in some basal
asterids. For example, Plerandra strongly resembles Deinanthe (Hydrangeaceae: Cor-
nales) in its mode of androecium initiation (Hufford 1998). Moreover, stamens of
adjacent whorls in Deinanthe sometimes lie on the same radii (Hufford 1998, Fig. 23),
as we observed in Plerandra.

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2. Meristic variation.
(A) Isomery. Isomerous (i.e., those with equal number of sepals, petals, stamens
and carpels) flowers are very common in Araliaceae. Among isomerous flowers, pen-
tamery is most common. Pentamerous flowers appear to be primitive within Araliace-
ae. However, members of many basal lineages (Fig. 37) have bicarpellate gynoecium
in otherwise pentamerous flowers (B1, see below), and this condition could be more
archaic than isomerous pentamery.
Although pentamery is common, other types of isomerous flowers occur in Arali-
aceae. Tetramerous flowers (along with pentamerous ones) occasionally occur in some
species of Oreopanax, Gamblea, Schefflera (S. venulosa) and Meryta (Smith 1985).
Flowers with increased merism are fairly common. For example, hexamerous flowers
occasionally occur in some Schefflera species with normally pentamerous flowers (e.g.
S. venulosa). The number of floral parts in isomerous whorls can reach 11–12 in Treve-
sia, Reynoldsia (Eyde & Tseng 1971) and some Schefflera species (e.g. S. actinophyl-
la). Several genera show extremely polymerous flowers, e.g. Tupidanthus calyptratus
(50–200-mery), Scheffleropsis spp. (up to 30-mery), Osmoxylon spp. (up to 30-mery).
However, we should note that the flower of Tupidanthus calyptratus cannot be viewed
as clearly isomerous because of the uncertainty regarding the merism of the corolla
and the calyx in this species. For the same reason, we cannot define whether or not this
flower is polystemonous, because the polyandry is the condition where the number of
stamens exceeds the number of all perianth organs (e.g., Hufford 1998, Endress 2003).
The uncertainty regarding the merism of the perianth in Tupidanthus is not due to the
lack of appropriate data. Sokoloff et al. (2007) and Nuraliev et al. (2009) studied flow-
er initiation and vascular anatomy of Tupidanthus in detail, but these data do not allow
counting their petals and sepals. A detailed comparison of corolla vasculature in Tupi-
danthus and in related Schefflera species did not allow establishing homologies be-
tween them (Nuraliev et al. 2009).
Loss of isomery often occurs in polymerous flowers due to unstable organ number
in all whorls (e.g. Tupidanthus — with respect to stamens and carpels, Schefflera acti-
nophylla). In these flowers, the number of elements is not strictly the same but nearly
equal in different whorls; in other words, the difference between whorls is much less
than merism of each whorl. This state can be described as partial isomery.
(B) The flower is not isomerous due to carpel number only.
(B1) Oligomerous gynoecium. The gynoecium of two (sometimes three) carpels
associated with pentamerous corolla and androecium is the common within Araliaceae
and occurs in several lineages of this family such as Astrotricha, Polyscias, Brassaiop-
sis, Eleutherococcus, etc. Although tetramery of corolla and androecium is a typical
condition for Tetrapanax, its flower has two carpels and hence it is not isomerous
(Eyde & Tseng 1971).
Molecular data (see also Fig. 37) suggest that the bicarpellate gynoecium is an an-
cestral condition in core Araliaceae (Plunkett et al. 1996, 1997, 2004b), but consider-
able infrafamiliar and even infrageneric variability of carpel number makes this idea
questionable (Wen et al. 2001).
(B2) Polymerous gynoecium. Increase of carpel number relative to the merism of
other whorls occurs in several unrelated clades of Araliaceae (Fig. 37), for example, in

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 M.S. Nuraliev et al., Flowers of Araliaceae 261

Fig. 37. Mapping of flower merism on the simplified phylogenetic tree based on Bayesian inference
analysis of the combined (ITS and trnL-trnF) data for Araliaceae (Plunkett et al. 2004b). G=gynoecium,
A=androecium, C=corolla. Large boxes show taxa where flower groundplan is typical for euasterds,
i.e. corolla and androecium are 4–5(6)-merous and gynoecium is (1)2–5(6)-merous. Information on
floral merism was taken from Bamps (1974), Bean (1997), Eyde & Tseng (1971), Jebb (1998), Harms
(1898), Lowry (1990), Marais (1984), Philipson (1965, 1995), Reyneke (1981), Shang & Lowry
(2007), Smith & Stone (1968), Smith (1985), Sosa (1979), Tennant (1968), Viguier (1910–1913), and
personal observations.

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262 M.S. Nuraliev et al., Flowers of Araliaceae

Fatsia polycarpa, Schefflera gabriellae. Note the species Schefflera octophylla with
the same phenomenon is not included in the figure 37 because of its absence from the
phylogenetic tree used for the figure.
(C) The flower is not isomerous due to polymery of its single-whorled androecium.
This condition occurs in some species of closely related genera Tetraplasandra and
Gastonia (Philipson 1979), for example in Gastonia spectabilis (Fig. 37) and in Tetra-
plasandra waialealae studied here (not on Fig. 37). The combination of polymerous
androecium with oligomerous gynoecium and corolla was regarded by Cronquist
(1981, 1988) as one of the possible ancestral conditions for Araliaceae. Interestingly,
the carpels of Tetraplasandra (at least T. waialealae) often alternate with petals or the
orientation of these two whorls is not correlated, whereas in isomerous flowers of
other Araliaceae petals and carpels lie on the same radii. A polymerous androecium is
a rare feature for euasterids, but occurs quite often in basal asterids. For instance, Car-
penteria (Hydrangeaceae, Cornales) possesses extremely specific polyandrous flow-
ers. The androecium of Carpenteria develops as single-whorled but looks like consist-
ing of several whorls in mature flowers (Hufford 1998).
Among euasterids, an interesting case of co-occurrence of isomerous and non-
isomerous flowers due to the meristic variations of androecium is reported for Theligo-
num cynocrambe (Rutishauser et al. 1998). This member of Rubiaceae is characterized
by unisexual flowers. Its male flowers bear only two or three perianth parts but their
stamen number varies considerably within inflorescence depending on a flower posi-
tion in floral cluster. Some of male flowers are isomerous, with only two or three sta-
mens in alternipetalous position which are initiated as individual primordia. In non-
isomerous male flowers, however, more numerous (up to 19) stamens are arranged into
a single whorl. In such flowers, the androecium is initiated as a continuous rim divid-
ing further into individual stamen primordia. In mature flowers some stamens of a
whorl become occasionally displaced to the centre or periphery giving impression of
several stamen whorls (Rutishauser et al., 1998).
Increasing stamen number in Tetraplasandra flowers could occur by at least two
different ways: (1) by increasing merism of the androecium, i.e., by a simple multipli-
cation of stamen primordia within stamen whorl and (2) by stamen multiplication from
antesepalous sectors which results in development of a fascicle of stamens instead of a
single stamen from each androecium primordium. The last case can be found in poly-
androus flowers of some eudicots (e.g. Ronse De Craene & Smets 1991). The presence
or absence of stamen groups should be verified by investigations of early flower devel-
opment (development of several stamens from antesepalous common primordia) and
flower vascular anatomy (presence of stamen trunk bundles). Although we had only
very limited material for stages younger than illustrated in Fig. 25, our preliminary
data suggest absence of common stamen primordia in Tetraplasandra.
3. Congenital petal fusion (Tupidanthus calyptratus, Osmoxylon spp.). Presence of
the corolla tube is a key feature of the asterid clade, but in Tupidanthus the sympeta-
lous corolla is transformed into a calyptra and is very distinctive from the typical
asterid corolla tube in terms of its shape and function (see Sokoloff et al. 2007).
4. Variation of flower shape. The flower of Schefflera actinophylla changes its shape
during the development from strongly polysymmetric to slightly disymmetric, in other

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 M.S. Nuraliev et al., Flowers of Araliaceae 263

words, the flowers are disymmetric with early polysymmetry (sensu Endress 1999). At
the same time, the orientation of the symmetry plane here does not depend from the
position of structures surrounding the flower, such as the flower subtending bract and
the bracteoles. On the other hand, in mature flowers, symmetry plane of carpel and
petal arrangement finely correspond to each other and to the symmetry plane of the
entire flower. This combination of features means that the formation of disymmetry is
seemingly triggered by minor differences in growth rates of different sectors of a flow-
er. It is unclear whether these differences in growth rates are due to space available in
the entire growing inflorescence with closely spaced flowers.
The complicate receptacle shape in Tupidanthus allows insertion of a huge number
of stamens and carpels in a single whorl each and facilitates compitum formation
(Sokoloff et al. 2007). In some other taxa with less polymerous gynoecium (Osmoxy-
lon, Munroidendron, some Schefflera species), carpel margins in symplicate zone tend
to be postgenitally united in the center of the flower along a line rather than just in a
central point (see also Endress 2006). This resembles the condition in Tupidanthus,
though in a less pronounced form. However, our observations on Schefflera actino-
phylla, which is phylogenetically relatively close to Tupidanthus, show that its recep-
tacle is circular and the overall flower shape remains circular until the development of
the symplicate gynoecium zone. Therefore, the flower receptacle provides enough
space for initiation of numerous organs (12 in each whorl), and the spatial difficulty
appears only at the stage of organ joining (carpels to form a compitum and petals to
protect the floral bud). This condition might be regarded as a logical step (but not nec-
essarily a real intermediate form!) toward the Tupidanthus gynoecium where the sym-
metry is determined at early developmental stages (the flower is disymmetric or some-
times asymmetric sensu Endress, 1999). There is no doubt that the flower shape is
strongly connected with flower merism and non-polysymmetric flowers are derived
from polysymmetric. Therefore, disymmetric flower of Tupidanthus most likely
evolved by disruption of flower polysymmetry of its ancestor. This is an argument for
secondary origin of polymerous flowers.
Unusual floral symmetry in Schefflera actinophylla and Tupidanthus is to compare
with that of disymmetric or even asymmetric mature flowers in Euptelea (Eupteleace-
ae: Ranunculales) (Ren et al. 2007). Unlike Tupidanthus, however, the flower of Eupt-
elea is wider in a transverse plane than in a median plane, thus its symmetry is deter-
mined by external reasons, namely by pressure of the bract. Euptelea is also distinctive
in non-simultaneous development of stamens as well as carpels, which causes so-
called early flower asymmetry in this species. To summarize, we can mark out several
reasons for changing flower symmetry such as external pressure and unevenness of
androecium and/gynoecium development (Euptelea), connection of organs in the cen-
tre of flower, including development of the compitum (Schefflera actinophylla and
Tupidanthus), and arrangement of multiple organ primordia in one whorl at the limited
size of flower meristem (Tupidanthus).
Among euasterids, bisymmetric flowers with increased stamen number are reported
also from Theligonum cynocrambe (Rubiaceae), where numerous stamens can form an
elliptic whorl (Rutishauser et al. 1998), which slightly reminiscent the androecium
structure of Tupidanthus.

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264 M.S. Nuraliev et al., Flowers of Araliaceae

Floral polymery as a derived feature in Araliaceae

It is most likely that the polymery of flowers, which was often considered to be primi-
tive for angiosperms in general and for Araliaceae in particular (e.g., Harms 1898,
Viguier 1906, Li 1942, Takhtajan 1966, Grushvitsky & Skvortsova 1973, Grushvitsky
1981), is a derived condition within Apiales. Polymery as such, does not represent a
single character state in Araliaceae. Our study revealed several different characters that
should be considered separately. Several kinds of so-called “polymerous flowers” can
be detected. These include (hemi)isomerous polymerous flowers, as in Schefflera acti-
nophylla, flowers with (hemi)isomerous polymerous gynoecia and androecia and un-
defined merism of the perianth (Tupidanthus), flowers with one-whorled polymerous
androecia and oligomerous perianth and gynoecia (Tetraplasandra), flowers with
polymerous and many-whorled androecia and polymerous one-whorled gynoecia
combined with oligomery in the perianth (Plerandra), and flowers with polymery con-
fined to the gynoecia (as in Schefflera octophylla). These different types of “polymer-
ous flowers” are found in different groups of Araliaceae, so they do not form a single
lineage. Therefore we should agree with conclusions based on character mapping onto
molecular phylogenies and propose tetracyclic pentamerous (possibly except the
bicarpellate gynoecium) flower with semi-inferior ovary as ancestral for Araliaceae.
Thus, we also agree with the earlier view by Cronquist (1968, 1981, 1989) based on
comparative morphology. Deviations from tetracycly occur rarely and are probably
connected with deviations in flower merism. That is why we suppose these species to
be derived from species with tetracyclic flowers. Similar reasoning can be applied to
petal fusion. According to the discussion above we should consider taxa with highly
polymerous flowers (Tupidanthus calyptratus, Plerandra spp., Tetraplasandra spp.,
Osmoxylon spp.) as highly derived species which originated from a pentamerous ara-
liaceous ancestor and evolved in a very distinct way from the main evolutionary trend
of euasterid flowers.

Future questions

This survey of the flower groundplan variation within Araliaceae suggests two ques-
tions that should be answered by further investigations:
1. Why are flowers of Araliaceae so diverse and those of Umbelliferae so uniform?
In the framework of traditional views on taxonomic placement of these families, there
was a possibility to assume that Araliaceae retained a kind of primitive polymorphism,
and the floral structure is more canalized in the more advanced family, Umbelliferae.
Current molecular phylogenetic data are congruent with the idea of primitiveness of
pentamerous flowers (possibly with dimerous gynoecium) within the Araliaceae-Um-
belliferae complex (Plunkett et al. 1997, Plunkett et al. 2004a, Sokoloff et al. 2007).
Traits of floral polymery appeared several times in the evolution of Araliaceae. This is
clear not only from mapping cases of floral polymery onto molecular trees of the fam-
ily but also from the fact that polymerous flowers of various Araliaceae are sharply
different from each other in terms of their groundplan. Flowers of Umbelliferae might

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 M.S. Nuraliev et al., Flowers of Araliaceae 265

be so stable because the dimery of the gynoecium is of functional significance due to

the special fruit type, but this does not explain presence of a homoplastic tendency in
Araliaceae.
2. Are general regularities of spatial pattern formation in developing flowers con-
servative across Araliaceae and Umbelliferae? More precisely, what is the relative
impact of acropetal and basipetal patterning (sensu Choob & Penin (2004) and Penin
et al. (2004); see also Sokoloff et al. 2008) in floral initiation in different taxa within
these families? Stable orientation of the two carpels in the median plane of the flower
and occasional loss of the calyx suggest an important role of basipetal patterning in
Umbelliferae. Our observations on androecium and gynoecium variation in Tupidan-
thus suggest patterning of carpel sites before those of stamens (Sokoloff et al. 2007).
However, such cases as the co-occurrence of sepals and petals in two regularly alter-
nating oligomerous whorls in flowers with increased and unstable stamen number, and
especially the presence of multiple carpels in otherwise pentamerous flower (e.g.
Schefflera octophylla) can hardly be explained by the basipetal patterning model. Ob-
viously, these data show some diversity in interplay between basipetal and acropetal
patterning within Apiales that needs more detailed analysis. An important observation
is variable relative position of petals and carpels in Tetraplasandra (i.e., some flowers
are with antepetalous carpels and other are with alternipetalous carpels). This suggests
independent patterning of gynoecium and perianth in Tetraplasandra. Certainly, flow-
ers of Araliaceae could be an interesting subject for evo-devo investigations.

Conclusions
1. Although floral pentamery (at least in the perianth and androecium) is common
within Araliaceae, almost no floral morphological features are constant. Invariable fea-
tures are: whorl element arrangement, presence of a corolla, free stamens, syncarpous
one-whorled gynoecium.
2. As a wide range of non-pentamerous flowers in Araliaceae suggests, deviations
from the pentamerous groundplan occur independently in different groups of this fam-
ily.
3. At least four major cases of evolutionary polymerization of flower occur in the
family: the Asian Schefflera clade (incl. Tupidanthus), the Pacific Schefflera clade
(incl. Plerandra), Polyscias-Tetraplasandra group, and Osmoxylon.
4. The following main trends of floral evolution can be distinguished: reduction of
calyx, increase of stamen number and increase of carpel number with changing flower
symmetry.

Acknowledgements

We are sincerely thankful to Peter K. Endress, Peter Leins and Louis Ronse De Craene for important
and very helpful comments on the manuscript, to Mark W. Chase for discussion on Hoplestigma, to
David H. Lorence (Natural Tropical Botanical Garden, Kalaheo, USA), Porter P. Lowry II (Missouri
Botanical Garden, St. Louis, USA), Gregory M. Plunkett (Virginia Commonwealth University, Rich-

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266 M.S. Nuraliev et al., Flowers of Araliaceae

mond, USA), Armen L. Takhtajan (Komarov Botanical Institute, St. Petersburg, Russia), Anton S.
Beer (Moscow State University, Moscow, Russia) for help in obtaining plant material and/or helpful
discussion and the staff of the Interdepartmental Laboratory of Electronic Microscopy (Moscow State
University) for their kind help with the SEM investigations. The work was supported by the Russian
Foundation of Basic Research (grants no. 06-04-48003-a and 06-04-48113-a), and partially by the
President of Russia (grant no. MD-2644.2009.4).

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Addresses of the authors:

Maxim Nuraliev, Prof. Dr. Dmitry Sokoloff, Dr. Margarita Remizowa, Department of Higher
Plants, Biological Faculty, Moscow State University, 119991 Moscow, Russia, email: max.
nuraliev@gmail.com
Dr. Alexei Oskolski, Botanical Museum, V.L. Komarov Botanical Institute of the Russian Acade-
my of Sciences, 2, Prof. Popov str. 197376 St. Petersburg, Russia.

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